Anim. Behav.

, 1991, 42, 993-1005

Parent/offspring conflict and maternal investment in rhesus macaques

MONTSERRAT GOMENDIO
Sub-Department of Animal Behaviour, University of Cambridge, High Street, Madingley,
Cambridge CB3 8AA, U.K.

(Received10 August 1990; initial acceptance18 October1990;

final acceptance 15 May 1991; MS. number:3629)

Abstract. Infant rhesus macaques, Macaca mulatta, gained access to their mothers' nipples less frequently
as they aged. At most ages, this decline was mainly a consequence of a decrease in infants' demands, and
also of increases in maternal rejections. When mothers first came into oestrus, however, infants intensified
their demands and became distressed, while mothers became more rejecting. These behavioural changes
resulted in no changes in suckling measures. Indeed during the breeding season suckling measures were
more stable than at any other time. Thus, behavioural conflict did not arise as a result of weaning, or as a
result of mothers enforcing a decrease in suckling frequency. Differences in suckling measures between
mothers who conceived and those who did not were not related to differences in demanding behaviour on
the part of infants, but rather to differences in maternal behaviour. Thus, while infants in both groups did
not differ in their frequency of attempts to gain access to the nipple, mothers who did conceive were more
rejecting, particularly during the breeding season, than mothers who did not conceive. The lower rejection
rates among the latter allowed an increase in suckling frequency during the breeding season, which
prevented their reproduction. It is suggested that less rejecting mothers did not reproduce in an attempt to
ensure their infants' survival.

Among mammals females are bound by their physi-
ology to provide most of the care that offspring
need, since it is females who become pregnant and
lactate. Mammalian females allocate most of their
reproductive effort into raising their offspring and
ensuring their survival, and in order to do this
successfully they have to obtain enough food
resources, which they transform into milk, to
satisfy their infants' needs. Lactation is an energeti-
cally costly activity and the costs increase as infants
grow heavier (Martin 1984; Oftedal 1984; Prentice
& Whitehead 1987). In an effort to cope with these
energy costs, lactating famales tend to increase the
time they spend feeding by using up time that would
otherwise be devoted to resting or to interacting
socially with other group members (Altmann t980,
1983; Clutton-Brock et al. 1982; Dunbar & Dunbar
1988). Despite this extra feeding time lactating
females still lose weight throughout lactation, and
show higher mortality rates and are less fertile than
non-lactating females (Altmann 1983; Bercovitch
1987; Clutton-Brock et al. 1989). Thus, females
incur considerable energy, reproductive and social
costs when raising their infants, and these costs
become exacerbated under poor nutritional con-
ditions (Lee 1987; Hauser & Fairbanks 1988). On
the other hand, young mammals suffer high mor-
tality rates and individual differences in offspring
survival are one of the major determinants of vari-
ation in female reproductive success (Clutton-
Brock 1988). Among large, slowly reproducing
mammals, which produce single offspring and
show extended maternal care, the survival of each
offspring represents a substantial proportion of a
female's reproductive output (e.g. red deer, Cervus
elaphus: Clutton-Brock et al. 1988; elephant seals,
Mirounga angirostris: Le Boeuf& Reiter 1988; pri-
mates: Altmann et al. 1988; Cheney et al. 1988). In
these species, minimum levels of maternal care will
be determined to some extent by offspring sur-
vival, and maximum levels by the reproductive or
survival costs incurred by mothers.
It is in the females' interest to balance the benefits
and costs of caring for each of their offspring so as
to maximize their lifetime reproductive success.
The optimal level of investment for a mother might
not, however, coincide with the optimum for her
offspring. Parent/offspring conflict theory postu-
lates that mothers and offspring are bound to dis-
agree over the amount of parental investment, so
that offspring will be selected to demand more
investment (and for longer) than mothers are

0003-3472/91 / ! 20993 + 13 $03.00/0 O 1991 The Association for the Study of Animal Behaviour
993
 994 Animal Behaviour, 42, 6
selected to provide (Trivers t974). The underlying
cause of this disagreement is a genetic conflict of
interests. Since mothers are equally related to all
their offspring, mothers are expected to end their
investment when the cost to themselves exceeds the
benefit to their young. The offspring, on the other
hand, are completely related to themselves and only
partly to their future siblings, and thus would be
expected to demand care until the cost to the
mother is more than twice the benefit to themselves
in the case of full-siblings, or more than four times
the benefit to themselves if other siblings are half-
siblings. Theoretical models have shown that the
evolution of demanding behaviour on the part of the
offspring that decreases parental fitness is indeed
possible (MacNair & Parker 1978; Parker &
MacNair 1978, 1979; Stamps et al. 1978).
Despite widespread interest in parent/offspring
conflict theory, few empirical studies have addressed
the issue. This is partly due to the scarcity of testable
predictions that can be derived from the original
theory. So far two general predictions have been
supported by empirical evidence. First, the existence
of parent/offspring conflict has been confirmed in
several species (see review in Trivets 1985); and
second, it has been shown that demanding offspring
can manipulate parents into providing more invest-
ment (Stamps et al. 1985). While in theory the model
makes specific predictions about the period during
parental investment in which parent/offspring con-
flict should occur, in practice this is virtually im-
possible to work out owing to the inherent diffi-
culties involved in measuring reproductive costs and
benefits with the accuracy that the model requires.
In primates mother-infant dyads typically
undergo marked phases of behavioural conflict,
which are characterized by high levels of maternal
rejections and infant distress (Hinde 1974; Clark
1977; Nash 1978; Altmann 1980; Lee 1987). It has
been widely assumed that this behavioural conflict
arises mainly as a consequence of mothers enforcing
nutritional independence upon their reluctant
infants, and it has therefore been equated with
weaning conflict (e.g. Trivers 1974, 1985; Clark
1977; Nash 1978; review in Nicolson 1987). Recent
work has shown that a high frequency of nipple
stimulation resulting from infant suckling depresses
maternal fertility and is thus a good measure of
maternal investment (sensu Trivers 1972; Nicolson
1982; Lee 1987; Stewart 1988; Gomendio 1989a).
This evidence has been incorporated into the pre-
vious argument, and it has been proposed that
behavioural conflict may arise when mothers start
limiting their infants' access to the nipple in order to
be able to conceive again while their infants try to
prevent this from happening (Lee 1987; Worlein
et al. 1988). This kind of conflict could be particu-
larly acute among seasonally breeding primates,
because females can conceive only during a limited
period of time in any given year. These ideas have
remained largely untested given the scarcity of
studies in which detailed suckling measures have
been collected.
My aim in this paper is to examine the nature and
timing of behavioural conflict in a seasonally breed-
ing primate and to relate it to changes in measures
of maternal investment. Particular attention is
paid to changes occurring during the first breeding
season after the birth of the infant, when the diver-
gent interests of mothers and infants may become
more apparent. Finally, since previous work has
shown that there were clear differences in suckling
patterns between mothers who conceived during
the next breeding season and those who did not
(Gomedio 1989a), I try to elucidate the behavioural
differences that gave rise to these differences in
suckling patterns.
METHODS
The Madingley Colony
The Madingley colony of rhesus macaques,
Macaca mulatta, has six social groups, each of them
consisting of a single adult male with several
females and their offspring. To maintain a situation
as similar as possible to the social structure and
social dynamics found among wild populations
(reviewed in Melnick & Pearl 1987; Dunbar 1988),
females are kept in their natal groups, which has led
to the formation of matrilines, while young males
are removed at the age of 3~, years. The adult male
in each group in regularly replaced to prevent
inbreeding.
Each social group inhabits an independent
enclosure, and all the monkeys have ample visual,
olfactory and auditory communication with mem-
bers of the other social groups. Each enclosure has
an outdoor pen (approximately 8 x 3 x 4 m) and a
heated indoor room (approximately 2.5 x 1.5 x
2 m). The animals are fed early in the morning with
pelleted monkey food, nuts and sunflower seeds,
and for a second time between 1300 and 1400 hours
with fresh fruit and vegetables.
 Gomendio: Parent/offspring conflict in macaques
Reproductive Data
Macaques are seasonal breeders (Vandenbergh
& Vessey 1968; Drickamer 1974; Gordon 1981;
Walker et al. 1983). At Madingtey, mating takes
place during autumn and winter, and females give
birth during spring and summer. The mating season
lasts for about 3 months, as in most macaque
populations (Melnick & Pearl 1987).
Although changes in the colour of the perineal
skin has been reported to occur around ovulation in
rhesus monkeys (Czaja et al. 1975), at Madingley
individuals vary greatly in this respect. In most
cases, no clear external morphological changes can
be detected, so female reproductive condition has
to be inferred from the females' behaviour. Thus, I
use the term 'oestrus' to refer only to the appear-
ance ofproceptive and receptive behaviour, leading
to copulatory behaviour with the male (see Hrdy &
Whitten 1987). No attempt was made to determine
whether ovulation accompanied a given oestrous
period. In rhesus macaques ovarian cycles last for
29 days and females are sexually receptive for 8-1 l
days (see Hrdy & Whitten 1987). All mature
females come into oestrus every breeding season,
but not all of them conceive every year. The first
day in which a female was seen in oestrus was con-
sidered as the start of the mating season for the
whole colony. For each female, the first day in
which she was observed interacting sexually with
the male was taken as the beginning of her first
oestrous period. Generally, females underwent
several consecutive oestrous periods before they
became pregnant, and on some occasions females
interacted sexually with the male after they had
already conceived. Conception dates were calcu-
lated by counting back 168 days from the date of
birth (van Wagenen 1972; Wilson et al. 1988).
I collected data on the timing of oestrous cycles
for all the colony females during the mating seasons
of 1985/1986 and 1986/1987. For this purpose, I
made systematic observations daily on all groups in
order to determine which females were in oestrus
throughout the season.
Behavioural Data
I collected behavioural data from August 1986
until August 1987 for 12 macaque infants (six males
and six females) born in 1986. Observations were
made from 1000 to 1300 hours and from 1400 hours
to sunset.
995
Data were collected from the age of 4 months
until the end of the first year of life. Each month of
age was divided into two 15-day long periods for
each infant. In each of these half-month periods I
collected six focal samples (Altmann 1974) for each
infant. As the focal samples were 10 min long, l-h
focal data were collected for each infant per fort-
night. The following rules were established for the
collection of data: (1) no more than three focal
samples would be collected in any one day on the
same individual; (2) at least 10 rain had to elapse
between two consecutive focal samples on the same
individual; (3) focal sampling would not be started
on individuals when they were asleep, and a focal
sample would be discarded if the infant had been
asleep for more than 5 min (half the duration of the
focal sample); (4) feeding times were avoided; and
(5) when a mother was in oestrus observations on
her infant were intensified up to six focal samples in
any one day. If under these circumstances more
than three focal samples were collected on the same
individual on a given day, they were divided into
morning and afternoon sessions. If six focal
samples were collected on 1 day for an infant, more
focal samples were collected later on during that
half-month period. During focal sampling all social
interactions were recorded continuously, together
with the identity of the partner(s). Other behaviour
that did not fall into the social category strictly
speaking, such as distress vocalizations, was also
recorded.
I analysed the following behavioural variables.
(1) Successful attempts at the nipple: those
instances in which infants gained access to the
nipple and remained there for longer that 5 s. It is
worth mentioning that the mothers normally either
rejected their infants' attempts straight away, or
allowed them to stay on the nipple for considerably
longer periods, rendering this initial distinction
unnecessary.
(2) Rejections: those instances in which mothers
prevented their infants' attempts to gain access to
the nipple. It includes 'passive' (obstructing access
to the nipple with an arm, pulling the nipples up or
making a slight movement away from the infant)
and 'active' (pushing the infant away or being
aggressive towards the infant) rejections.
(3) Infant distressed: infants were considered to
be distressed when they jerked, geckered (i.e.
vocalized), whooed, squeaked, screamed or had
tantrums. Only distress that was a consequence of a
neglecting or rejecting attitude on the part of
996 Animal Behaviour, 42, 6
mothers was included in the analyses. Thus, distress
caused by aggression received from others was not
taken into account here.
Derived measures were calculated by combining
the previous absolute measures in the following
ways.
(1) Total number of attempts to gain access to
the nipple: the sum of the frequency of successful
attempts and the frequency of rejections.
(2) Relative frequency of rejections: this was
determined by dividing the frequency of rejections
by the frequency of total attempts. This variable
reflects the proportion of attempts that are rejected
by the mother. It should be noted that the inverse of
this measure, or the same measure but represented in
inverse order on the Y-axis, has been used in other
studies (Lee 1987) under the name of 'suckling
success'.
Analyses
All these behavioural categories, except infant
distress, were treated as 'events'. Thus, absolute
frequencies were obtained from the focal samples.
Infant distress was normally too prolonged to be
treated as an event, making the use of frequencies
somewhat misleading. I felt the best way of analys-
ing this variable would be to treat it as in one-zero
sampling, i.e. to determine whether it had occurred
or not during each of the 15-s periods in which the
focal periods were divided. The results are therefore
expressed as the proportion of all 15-s intervals in
which infants showed signs of distress (see Martin
& Bateson 1986 for a discussion of this technique).
Most results are presented in relation to months
of age. For each infant a mean value was obtained
for each month of age. To obtain a mean value for
the whole sample (or for a particular group of
infants) the combined mean of all the infants' indi-
vidual means was calculated. When analyses were
done in relation to the timing of specific repro-
ductive events, such as first oestrus or conception,
data from the month in which such an event took
place have been considered. When the results
include a broader time scale before and after these
events, this was done by including data from the
months that preceded and followed these events. In
this case, the age period in which first oestrus or
conception occurred is referred to as point '0', the
preceding and following age periods as - 1 and + 1
months, and so on.
Statistical tests include non-parametric tests such
as the Mann-Whitney test and Spearman rank
correlation coefficient. ANOVA was used to
examine the effect of some factors throughout the
whole age range, and to compare different cat-
egories of individuals. For this purpose, all the
behavioural variables were tested for normality
and, whenever they failed to fulfil this requirement,
data were transformed by using square-root trans-
formations in the case of frequencies, and arcsine-
square root transformations in the case of pro-
portions or percentages (Martin & Bateson 1986).
Transformed data were then re-tested for normality,
satisfying the tests in all cases. All probabilities were
two-tailed.
RESULTS
Developmental Changes
At the age of 4 months rhesus macaque infants
tried to gain access to the nipple about 20 times
per h (Fig. la). The frequency of attempts
decreased to about 15 during the next month, but it
subsequently increased again, reaching a high
plateau from 7 to 8 months, which was followed by
a gradual decline. No significant effect of age on the
frequency of attempts was found (ANOVA, F 8 =
0.652, NS). The high plateau present at 7 and 8
months is particularly relevant since it coincides
with the average age at the time mothers came into
oestrus. Indeed, when the data were plotted in
relation to the timing of mothers' first oestrus, it
was found that infants were attempting to gain
access to the nipple significantly more frequently
when their mothers returned to oestrus than during
the previous month (Mann-Whitney, U=44,
N 1= 12, N 2 = 12, P = 0"05).
Infants gained access to the nipple less frequently
as they aged (Fig. lb; ANOVA, F8=4.373, P =
0-0002). This decrease was most marked between
months 4 and 5, and became more gradual there-
after. Despite the intensification of the infants'
attempts to gain the nipple when their mothers
came into oestrus, no significant changes in the fre-
quency of successful attempts occurred at this time
(Mann Whitney, U = 57-5, N 1= 12, N 2 = 12, NS).
The decline in the frequency of successful
attempts was associated with an increase in
maternal rejections with age (Fig. lc). Mothers
steadily increased the frequency with which they
rejected their infants until reaching a plateau from
the age of 8 months onwards, and became only
slightly less rejecting when their infants were 12
 Gomendio: Parent/offspring conflict in macaques 997

(a) (b)
201

15

I0 .~ 0

(,9
5 84

l I I J I I I I I 0 I l l l l l l l l

All re ec'i'ed
2 0 - - 1.0
(e) (d)

0.8
15

.o 0'6
o
m

E 0"4

5
0.2

o I I I I I I t I I o.o I I I I I I 1 I I
4 5 6 7 8 9 I0 I1 12 None 4 5 6 7 8 9 I0 II 12
re jet fed
Infant's age (months)

Figure 1. Developmental courses of: (a) frequency of attempts to gain access to the nipple made by the infants; (b)
frequency of successful attempts to gain access to the nipple; (c) frequency of maternal rejections; and (d) relative
rejections (frequency of rejections/frequency of attempts). Values are means. N = 12.

months old ( A N O V A , F s = 1.488, Ns). The increase
in rejections when mothers came into oestrus was
statistically significant ( U = 4 2 . 5 , N 1 = 12, N 2 = 12,
P=0-04). The relative frequency of rejections,
which reflects the ratio of rejections per number of
attempts made, shows that a greater proportion of
the infants' attempts were rejected as the infants
aged, the increase being particularly marked from 4
to 5 months of age (Fig. ld; A N O V A , F8=5,87,
P=0-0001).
Finally, low levels of infant distress at young ages
were followed by a sharp rise leading to a peak at 8
months, after which levels of distress decreased
again (Fig. 2; A N O V A , F 8 =0'865, Ns). Once again,
the peak at 8 months corresponds to a marked
increase in levels of infant distress at the time
mothers came into oestrus (Mann-Whitney, U =
41.5, N 1 = 12, N 2 = 12, P=0.03).
Correlations with Suckling Measures
F r o m 4 to 12 months of age, the frequency of
attempts made by the infants to gain the nipple, and
the frequency of successful attempts, were positively
998 Animal Behaviour, 42, 6
18
16
14
v in suckling patterns became particularly marked
I0
8 suckling patterns between conceivers and non-
o conceivers, the data for both groups were plotted
-= 6
0 I I I I I ] I I I
4 5 6 7 8 9 I0 II 12
Infant's age (months)
Figure 2. Changes in levelsof infant distress with age (as a
percentage of point samples). Values are means. N= 12.
correlated with both the frequency of suckling
bouts (Total attempts/h: r s = 0.55, N = 9, P = 0.05;
Successful attempts/h: rs = 0'933, N = 9, P = 0-004),
and the number of nipple contacts made per bout
(Total attempts/h: rs=0.533, N = 9 , P=0.06;
Successful attempts/h: rs= 0"85, P = 0"008). On the
other hand, both the absolute and relative frequency
of rejections were negatively correlated with the
frequency of suckling bouts (Rejections/h: rs=
-0.567, N = 9 , P=0.05; Relative rejections:
rs = - 0"867, N = 9, P = 0"007), and with the number
of nipple contacts per bout (Rejections/h: rs=
-0'567, N = 9 , P=0"05; Relative rejections: rs=
-0-767, N = 9 , P=0.01). In other words, at those
ages at which infants were making more attempts to
gain access to the nipple, and at which they were
achieving a higher frequency of successful
attempts, the frequency of suckling bouts and the
number of nipple contacts per bout were high. On
the other hand, frequent rejections, and a high pro-
portion of attempts rejected, were associated with
low suckling bout frequencies and few nipple con-
tacts per bout. Thus, the behavioural measures used
here are strongly associated with changes in suckling
patterns over age (see Gomendio 1989a). Not sur-
prisingly,the frequency of successful attempts seems
to be a very reliable correlate of suckling measures.
Coneeivers Versus Non-conceivers
Previous work has shown that mothers who con-
ceived during the mating season experienced a very
different suckling pattern from those females who
failed to conceive (Gomendio 1989a). Females who
did become pregnant again had a lower suckling
frequency and fewer nipple contacts per bout than
females who failed to conceive. These differences
during the mating season. To understand the
behavioural causes underlying the differences in
in relation to the first appearance of oestrus.
Additional information on the existence of differ-
ences throughout the whole age range is given
below.
Overall, infants ofconceivers and non-conceivers
did not differ in the frequency with which they
attempted to gain access to the nipple (two-way
ANOVA, Conceivers versus Non-conceivers: F 1 =
1.001, ys; Age: F=0.59, Ns). Around the mating
season infants in both groups behaved similarly.
During the preceding months infants decreased the
frequency of attempts, but when their mothers
returned to oestrus all infants dramatically
increased their attempts, and became less demand-
ing again during the following months (Fig. 3a). The
increase in attempts associated with the mothers'
first oestrus was more pronounced for infants of
non-conceivers (Mann-Whitney, U=2.5, N1 = 5,
N z = 5, P=0"01), who appeared to try to gain the
nipple more frequently when their mothers resumed
cycling than infants ofconceivers, although this was
not significant (Mann-Whitney, U = 10.5, N 1= 7,
N 2 = 5, NS).
Despite the fact that infants from the two groups
attempted to gain access to the nipple to the same
extent, throughout months 4-12 infants of con-
ceivers were successful less frequently than were
infants of non-conceivers (two-way ANOVA,
Conceivers versus Non-conceivers: F1=22-744 ,
P=0-0001, Age: F 1 =4.803, P = 0-0001). When the
data were plotted in relation to the mothers' return
to oestrus it was found that while infants of con-
ceivers showed a consistent and gradual decline,
infants of non-conceivers appeared to show an
increase in the frequency of successful attempts
when their mothers returned to oestrus, although
this was not quite significant (Mann-Whitney,
U=6, N 1 =5, N2=5, P=0.08; Fig. 3b). Infants of
non-conceiversgained the nipple 5 more times per h
than infants of conceivers when their mothers
returned to oestrus. The higher frequency among
infants of non-conceivers was maintained during
 Gomendio: Parent~offspring conflict in macaques 999

(a) (b
25--

2
20
~
15--
"6
"5
E
I0

~o

L
t I I I I I I ol I I I I I I I

1,0
(c (d

0.8 0

g
~. 0-6
(D
o

~ 0.4 o

0.2 5

0-0 I I I I 1 I .I o l I I I I I I
-3 -2 -I 0 I 2 3 -3 -2 -I 0 I 2 3

Months before/offer f i r s t oesi'rus

Figure 3. Changes in the behaviour of mothers and infants during the months preceding and following maternal first
oestrus (point 0). (a) Frequency of attempts to gain access to the nipple made by the infants; (b) frequency of successful
attempts to gain access to the nipple; (c) relative rejections (frequency of rejections/frequency of attempts); and (d)
frequency of maternal rejections. Values are means, Conceivers: [] N = 7, Non-eonceivers: III N = 5.

the following m o n t h s ( M a n n - W h i t n e y , M o n t h 0: of their infants' attempts t h a n mothers w h o did not

U = 10, N 1 = 7, N 2 -- 5, NS; M o n t h + 1: U = 8, N 1 =
7, N 2 = 5 , P = 0 . 0 6 ; M o n t h + 2 : U = l l , N 1 = 7 ,
N 2 = 5 , NS; M o n t h + 3 : U = 5 , N ~ = 7 , N 2 = 4 ,
P=0.04).
So far, the evidence shows t h a t as they aged
infants of conceivers were gaining access to the
nipple less frequently t h a n infants of n o n -
conceivers, despite the fact t h a t they did not m a k e
fewer attempts. The differences in success seem to
result fi'om m o t h e r s w h o conceived rejecting more
conceive (two-way A N O V A , Conceivers versus
Non-conceivers: F 1 -- 22.479, P = 0'0001; Age: F 8 =
6.818, P = 0 . 0 0 0 1 ) . In relation to the breeding
season, these differences became m o r e a p p a r e n t
from the time m o t h e r s returned to oestrus onwards
( M a n n - W h i t n e y , M o n t h 0: U = 12, N 1 = 7, N 2 = 5,
NS; M o n t h + 1 : U = 8 , N 1 = 7 , N 2 = 5 , P = 0 - 0 6 ;
M o n t h + 2: U = 9.5, NI = 7, N 2 = 5, NS; M o n t h + 3:
U = 4, N 1 = 7, N 2 = 4 , P = 0'02, Fig. 3c). Analyses o n
the absolute frequency of rejections s u p p o r t e d a n d
1000
2 0 - -
15
F got onto the nipple decreased more gradually. A
o
0 I I I I I
-5 -2 -I 0 I
Months b e f o r e / o t t e r
Figure 4. Changes in levels of infant distress during the
months preceding and following maternal first oestrus
(point 0). Values are means. Conceivers: D N=7,
Non-conceivers: 9 N= 5.
complemented these results. As already mentioned,
all mothers became more rejecting as they resumed
cycling, but mothers who conceived were more
rejecting and maintained higher levels of rejections
during the following months, while mothers who did
not conceive dropped their frequency of rejections
soon after returning to oestrus (Fig. 3d).
Finally, levels of infant distress in both groups did
not differ in relation to changes with age (two-way
ANOVA, Conceivers versus Non-conceivers: F 1=
0'035, NS; Age: F8-=0.905, NS; Interaction: F s =
0.625, NS). Infants ofconceivers and non-conceivers
shared a dramatic increase in levels of distress when
their mothers returned to oestrus, which gradually
decreased thereafter (Fig. 4).
DISCUSSION
In this study infants gained access to the nipple less
often as they aged. This pattern was the result of
changes in the behaviour of both mothers and in-
fants, but the responsibility of each partner in pro-
moting the reduction in suckling varied throughout
the age range considered. The most dramatic reduc-
tion in the frequency with which infants gained ac-
cess to the nipple occurred between months 4 and 5
of age, when infants experienced a decline from
about 15 times an hour to about 7. Infants were
primarily responsible for this decrease since they
made markedly fewer attempts to gain the nipple
Animal Behaviour, 42, 6
while mothers increased only slightly their fi'e-
quency of rejections. It is worth mentioning that it
is precisely at this age when solid foods become a
substantial part of an infant's diet (e.g. Altmann
1980). Thereafter, the frequency with which infants
m~ m particularly stable phase took place between
months 5 and 8 when the frequency of successful
attempts decreased remarkably little. During these
months infants tried to gain the nipple more and
more often, but these intensified demands were met
by increased maternal rejections, resulting in very
few changes in the actual frequency with which
infants got onto the nipple. This phase is particularly
I I important because for most infants it coincides with
2 5
the time when their mothers started coming into
f i r s t oestrus
oestrus. To find out whether the precise timing of the
resumption of oestrus by mothers could explain
more clearly changes in the behaviour of mothers
and infants, the month in which mothers came into
oestrus was compared with the previous month.
During their mothers' first oestrus infants signifi-
cantly increased the frequency of attempts while
mothers, on the other hand, significantly increased
the frequency of rejections, resulting in no changes
in the frequency of successful attempts. During
months 5-8 these behavioural changes were
accompanied by increasing signs of distress on the
part of infants. After month 8 the frequency of
successful attempts decreased somewhat more
rapidly, mainly as a result of infants reducing their
attempts, since the frequency of maternal rejections
remained fairly stable. It seems to be a rather wide-
spread phenomenon that low levels of maternal
rejections during the first months of life are
accompanied by considerable decreases in suckling
frequency (Altmann 1980; Nicolson 1982), sup-
porting the view that young infants play a substan-
tial role in attaining independence from their
mothers (Simpson & Simpson 1986; Simpson et al.
1986). A decrease in infants' attempts to gain the
nipple was in fact the main cause of the declining
levels of maternal investment during most of the
ages considered, except during the mating season
when infants escalated their demands.
Weaning was defined by Martin (1984) as 'the
phase of parental care during which the rate of
parental investment drops most sharply', and he
suggested that parental investment should be
measured as 'rate of milk transfer' or 'daily suck-
ling duration'. Since in primates it is the frequency
of nipple stimulation that affects the likelihood that
 Gomendio: Parent~offspring conflict in macaques
mothers will reproduce (Lee 1987; Gomendio
1989a), this seems to be the best behavioural
measure of maternal investment available. The
decrease in the frequency with which infants got
onto the nipple was somewhat more rapid from
month 4 to 5 than at older ages, but the change was
so gradual overall that it can be considered only as
one long continuum in which no abrupt changes can
be detected. Hence, rather than being a well defined
phase of sudden change, as Martin's definition
requires, weaning in cercopithecine primates seems
to comprise most of the long process of gradual
decline in maternal investment until the next sibling
is born (see also Nicolson 1982; Lee 1987).
Behavioural conflict intensifiedduring the mating
season, when infants tried to get onto the nipple
more often and showed frequent signs of distress,
and mothers became more rejecting. However,
these behavioural changes resulted in no changes
in the actual frequency with which infants gained
access to the nipple and, thus, were not related to
changes in levels of maternal investment (for more
detailed suckling measures see Gomendio 1989a).
Behavioural conflict, therefore, was not a conse-
quence of mothers forcing a reduction in the fre-
quency with which their infants got onto the nipple
in order to be able to conceive, and infants resisting,
as had been suggested (Lee 1987; Wortein et al.
1988). Intense behavioural conflict occurred during
a well defined and short period, which coincided
with the resumption of maternal oestrus, and which
was associated with no changes in suckling fre-
quency. The common assumption that nutritional
weaning or decreases in measures of maternal
investment are a major source of behaviourat con-
flict should be reconsidered. It should also be
emphasized that behavioural conflict was not a
consequence of the attainment of a minimal thres-
hold of maternal investment levels, because despite
further decreases in maternal investment after the
mating season, infants became less demanding and
less distressed. Furthermore, all infants became
demanding and distressed during the mating season,
despite great differences in suckling patterns and
maternal behaviour (see below). A brief review of
the literature reveals that the appearance of behav-
ioural conflict during the mating season seems to be
common in captive primate populations (Hinde
1974; Worlein et al. 1988), while in the wild conflict
tends to appear much earlier and long before
mothers resume sexual activity (Altmann 1980;
Nicolson 1982; Lee 1987). Altmann (1980) proposed
1001
that in wild populations behavioural conflict is
the result of a restructuring of suckling so as to
minimize interference with other maternal activi-
ties such as feeding and walking. It has also been
suggested that in highly social primates conflict
may arise when infant care limits the amount of
time that mothers can devote to other social
relationships that are crucial for the lifetime repro-
ductive success of females (Dunbar & Dunbar
1988). It is possible that the differences in the timing
of conflict between captive and wild populations
are the result of differences in maternal time
budgets and energy constraints. In captivity
mothers have plenty of time to spare which they can
devote to infant care, and interference between
other maternal activities and infants' demands may
occur only when mothers come into oestrus
because at this time mothers may shift their atten-
tion towards their sexual interactions with males
and towards the intensified levels of aggression
that break out among females (Eaton et al. 198t;
Johnson et al. 1982).
It could be argued that infants intensify their
demands for suckling at the time when mothers
come into oestrus so as to prevent them from repro-
ducing, and that mothers counteract by becoming
more rejecting. Against this interpretation stands
the fact that the increase in infants' demands takes
place only when mothers come into oestrus for the
first time, but infants' demands do not remain high
throughout the mating season which lasts for 3 4
months; thus, such a temporary increase is unlikely
to prevent maternal reproduction. The sudden
increase in infants' demands drops during the
following month, both for infants who have
succeeded in increasing their suckling rate and for
those who have not (see differences between con-
ceivers and non-conceivers below), giving further
support to the argument developed here. Other
studies have also reported increased demands for
suckling when mothers resume cycling as a response
to the abrupt changes in the behaviour of mothers
and other social partners that take place at this time
(Clark 1977; Nash 1978; Clutton-Brock et al. 1982;
Worlein et al. 1988).
It is nevertheless clear that differences in the
behaviour of mothers and infants had important
reproductive consequences for mothers. In the
study sample seven infants had mothers who con-
ceived again during the first mating season after
their birth and five had mothers who did not.
Mothers who reproduce experience lower suckling
1002 Animal Behaviour, 42, 6
frequencies and fewer nipple-contacts per bout than
mothers who fail to reproduce, and these differ-
ences become particularly marked during the
mating season (Gomendio 1989a). I now explore
which behavioural differences gave rise to these
differences in suckling patterns. According to
parent/offspring conflict theory it might be
expected that these differences were due to differ-
ences in the behaviour of the infants, such that
more demanding infants could have succeeded in
obtaining more maternal investment resulting in
reproductive failure for their mothers. The results
from this study suggest a different scenario.
The frequency with which infants got onto the
nipple was closely correlated with both the frequency
of suckling bouts and the number of attempts per
bout, and was thus a reliable indicator of these
suckling measures which influence maternal fer-
tility. Infants whose mothers conceived again
showed a gradual and consistent decline in the fre-
quency of successful attempts. Infants whose
mothers failed to conceive also showed an initial
decline with values similar to those of the other
group of infants, but experienced a dramatic
increase in the frequency of successful attempts
when their mothers first came into oestrus;
although this peak was followed by a marked drop,
they still gained access to the nipple more fre-
quently than the other group of infants from then
on (for detailed suckling measures see Gomendio
1989a). These differences were not the result of dif-
ferences in the behaviour of the infants, but rather
of differences in the behaviour of the mothers. No
differences were found in the behaviour of infants
whose mothers conceived and those whose mothers
did not. Both groups of infants followed a similar
pattern: they decreased their rate of attempts to get
onto the nipple first, and then intensified their
demands dramatically when their mothers returned
to oestrus; this peak was followed by a sudden drop
in both groups. The behaviour of both groups of
mothers was quite different. After showing similar
rejection rates during previous months, both
groups of mothers showed a sharp increase during
their first oestrus. This increase was more marked
for mothers who did conceive, and these mothers
maintained high levels of rejection during the fol-
lowing 3 months. In contrast, mothers who failed to
conceive decreased their frequency of rejections
during the following months until reaching pre-
oestrous values. Thus, all infants tried to get onto
the nipple more often during their mothers' first
oestrus. Mothers who responded by increasing
their levels of rejections and who maintained these
high levels during the mating season prevented
increases in suckling rates and were able to repro-
duce. Those mothers who did not increase their
rejection rate so much allowed an increase in nipple
stimulation during their first oestrus, and since
these mothers decreased their rejection rate during
the following months they maintained high levels of
nipple stimulation during the mating season and as
a consequence failed to conceive. Despite the differ-
ences in suckling rates and maternal behaviour,
infants in both groups became distressed during the
mating season. Other studies have shown that
rejecting mothers or mothers who wean their
infants early tend to give birth to their next infant
sooner (Simpson et al. 1981; Fairbanks & McGuire
1987; Lee 1987; Hauser & Fairbanks 1988).
It is likely that differences in levels of rejections
between mothers are related to mothers' percep-
tions of their infants, as well as to their own physi-
cal condition. The available evidence indicates that
mothers do in fact adjust their behaviour to their
infants' perceived needs: mothers with active
infants are more rejecting, presumably because
their infants are capable of coping with a certain
degree of independence (Simpson et al. 1981), and
mothers of twins provide more care to the weakest
infant of the pair (Spencer-Booth 1969; Klopfer &
Klopfer 1977). In this study, mothers who did not
conceive were either primiparous or subordinate
females with daughters. Infants of primiparous
mothers suffer high mortality rates (Hiraiwa 1981;
Nicolson 1987), and when they survive primiparous
mothers raise their infants at a great cost to them-
selves given their low body weight and small size,
and the additional energy requirements derived
from their own growth (Mori 1979; Anderson 1986;
Lancaster 1986; Gomendio 1989b). The daughters
of subordinate mothers are subjected to high levels
of aggression and tend to suffer high mortality rates
too (Dittus 1979; Silk et al. 1981; Silk 1988), so they
seem to need more maternal care and protection in
order to survive (Gomendio 1990; Gomendio et al.
1990). Among seasonally breeding eercopithecines
the decision to reproduce or not can be taken only
once each year, when infants are between 5 and 8
months old. I would argue that if infant survival is
at stake when the mating season takes place or if the
energetic strain on mothers is such that it threatens
the success of another reproductive attempt,
mothers choose to invest further in the current
 Gomendio: Parent/offspring conflict in macaques
infant at a reproductive cost to themselves. If, on
the other hand, infant survival is ensured and
mothers can physically afford reproducing again,
by maintaining high levels of rejections during the
breeding season mothers keep low levels of nipple
stimulation and re-conceive.
The situation described here shows many parallels
with that of wild populations under food limi-
tations. As happened to the primiparous mothers
and to the subordinate mothers with daughters in
this study, when infant survival is threatened by
food shortages and mothers experience difficulties
in coping with the energy costs of reproduction,
mothers delay the birth of their next infant
(primates: Lee 1987; Hauser & Fairbanks 1988; sea
mammals: Trillmich 1990); when food shortages
are so severe that maternal survival becomes
threatened, mothers may have little choice but to
neglect their infants.
The findings from this study thus challenge two
hypotheses which have been derived from parent/
offspring conflict theory. First, behavioural conflict
did not arise as a result of mothers reducing suck-
ling; and second, mothers who failed to conceive
did not have more demanding infants.
ACKNOWLEDGMENTS
Financial support came from a Research Student-
ship awarded by St John's College, Cambridge, and
from a Research Fellowship awarded by Trinity
Hall, Cambridge. I thank Michael Simpson for his
supervision of my work, and for allowing me access
to the colony data. David Rayment helped me to
identify the monkeys at the beginning, and looked
after them throughout the study. Saroj Datta,
Magdalena Janus, Davis Rayment and Michael
Simpson provided information on the reproductive
status of the females during the mating season.
Phyllis Lee gave me helpful advice throughout the
study. I am very grateful to Robert Hinde for his
constant support, and for permission to study the
colony, which is funded by the M.R.C. Robert
Hinde, Barry Keverne and Pat Bateson allowed
the use of facilities available at the Department.
I am grateful to Tim Clutton-Brock, Fernando
Colmenares, Robin Dunbar, Robert Hinde, Phyllis
Lee and Michael Simpson, for their helpful com-
ments on an earlier draft of the manuscript. I also
thank Eduardo Roldan for his constant help. The
manuscript was further improved by the suggestions
made by two referees.
1003
REFERENCES
Altmann, J. 1974. Observational study of behaviour:
samplingmethods. Behaviour, 49, 227-265.
Altmann, J. 1980. Baboon Mothers and Infants.
Cambridge, Massachusetts: Harvard University
Press.
Altmann, J. 1983.Costs of reproduction in baboons (Papio
cynoeephalus). In: Behavioural Energetics: the Cost of
Survival in Vertebrates (Ed. by W. P. Aspey & S. I.
Lustick), pp. 67-88. Columbus: Ohio State University
Press.
Altmann, J., Hausfater, G. & Altmann, S. A. 1988. Deter-
minants of reproductive success in savannah baboons,
Papio cynocephalus. In: Reproductive Success (Ed. by
T. H. Clutton-Brock), pp. 403~418. Chicago: The
Universityof Chicago Press.
Anderson, C. M. 1986. Female age: male preference and
reproductive success in primates. Int. J. Primatol., 7,
305 326.
Bercovitch, F. D. 1987. Female weight and reproductive
condition in a population of olive baboons (Papio
anubis). Am. J. Primatol., 12, 189-195.
Cheney, D. L., Seyfarth, R. M., Andelman, S. J. & Lee,
P. C. 1988.Reproductive successin vervetmonkeys. In:
Reproductive Success (Ed. by T. H. Clutton-Brock), pp.
384404. Chicago: The University of Chicago Press.
Clark, C. B. 1977. A preliminary report on weaning
among chimpanzees of the Gombe National Park,
Tanzania. In: Primate Bio-social Development (Ed. by
S. Chevalier-Skolnikoff& F. E. Poirier), pp. 235-260.
New York: Garland Press.
Clutton-Brock, T. H. 1988. Reproductive success. In:
Reproductive Suceess (Ed. by T. H. Clutton-Brock),
pp, 472~185. Chicago: The University of Chicago
Press.
Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E.
1988. Reproductive success in male and remale red
deer. In: Reproductive Success (Ed. by T. H. Clutton-
Brock), pp. 325-343. Chicago: The University of
Chicago Press.
Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E.
1989. Fitness costs of gestation and lactation in wild
mammals. Nature, Lond., 337, 260~62.
Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D.
1982. Red Deer. Behaviour and Ecology of the Two
Sexes. Edinburgh: Edinburgh University Press.
Czaja, J. A., Eisele, S. G. & Goy, R. W. 1975. Cyclical
changes in the sexual skin of femalerhesus:relationship
to mating behaviour and successful artificial insemi-
nation. Fedn. Proe. Fedn. Ann. Sots. exp. Biol., 34,1680
1684.
Dittus, W. P. J. 1979.The evolution of behaviours regulat-
ing density and age-specific sex ratios in a primate
population. Behaviour, 69, 265-302.
Drickamer, L. C. 1974. A ten-year summary of repro-
ductive data for free-ranging Macaea mulatta. Folia
primatol., 21, 61-80.
Dunbar, R. I. M. 1988. Primate Social Systems. London:
Croom Helm.
Dunbar, R. I. M. & Dunbar, R. 1988. Maternal time
budgets of gelada baboons. Anim. Behav., 36, 970-980.
 1004 Animal Behaviour, 42, 6
Eaton, G. G., Modahl, H. B. & Johnson, D. F. 1981.
Aggressive behavior in a confined troop of Japanese
macaques: effects of density, season, and gender.
Aggress. Behav., 7, 145 164.
Fairbanks, L. A. & McGuire, M. T. 1987. Mother-infant
relationships in vervet monkeys: response to new adult
males. Int. J. Primatol., 8, 351-366.
Gomendio, M. 1989a. Suckling behaviour and fertility in
rhesus macaques (Macaca mulatta). J. Zool., Lond.,
217, 449-467.
Gomendio, M. 1989b. Differences in fertility and suck-
ling patterns between primiparous and multiparous
rhesus mothers (Macaca mulatta). J. Reprod. Fert., 87,
529 542.
Gomendio, M. 1990. The influence of maternal rank, and
infant sex on maternal investment trends in macaques:
birth sex ratios, inter-birth intervals and suckling
patterns. Behav. Ecol. Sociobiol., 27, 365-375.
Gomendio, M., Clutton-Brock, T. H., Albon, S. D.,
Guinness, F. E. & Simpson, M. J. 1990. Mammalian
sex ratios and variation in costs of rearing sons and
daughters. Nature, Lond., 343, 261-263.
Gordon, T. P. 1981. Reproductive behavior in the rhesus
monkey: social and endocrine variables. Am. Zool., 21,
185 195.
Hauser, M. C. & Fairbanks, L. A. 1988. Mother-offspring
conflict in vervet monkeys: variation in response to eco-
logical conditions. Anim. Behav., 36, 802-813.
Hinde, R. A. 1974. Biological Bases of Human Social
Behavior. New York: McGraw Hill.
Hiraiwa, M. 1981. Maternal and alloparental care in a
troop of free-ranging Japanese monkeys. Primates, 22,
309-329.
Hrdy, S. B. & Whitten, P. L. 1987. Patterning of sexual
activity. In: Primate Societies (Ed. by B. B. Smuts, D. L.
Cheney, R. M. Seyfarth, R. W. Wrangham & T. T.
Struhsaker), pp. 37~384. Chicago: The University of
Chicago Press.
Johnson, D. F., Modahl, K. B. & Eaton G. G. 1982.
Dominance status of adult male Japanese macaques:
relationship to female dominance status, male mating
behaviour, seasonal changes and developmental
changes. Anim. Behav., 30, 383 392.
Klopfer, P. & Klopfer, M. 1977. Compensatory responses
of goat mothers to their impaired young. Anim. Behav.,
25, 286-291.
Lancaster, J. B. 1986. Human adolescence and repro-
duction: an evolutionary perspective. In: School-age
Pregnancy and Parenthood. Biosocial Dimensions (Ed.
by J. B. Lancaster & B. A. Hamburg), pp. 17-37. New
York: Aldine de Gruyter.
Le Boeuf, B. J. & Reiter, J. 1988. Lifetime reproductive
success in northern elephant seals. In: Reproductive
Success (Ed. by T. H. Clutton-Brock), pp. 344-362.
Chicago: The University of Chicago Press.
Lee, P. C. 1987. Nutrition, fertility and maternat invest-
ment in primates. J. Zool., Lond., 213, 409-422.
MacNair, M. R. & Parker, G. A. 1978. Models of parent-
offspring conflict. II. Promiscuity. Anim. Behav., 26,
111 122.
Martin, T. 1984. The meaning of weaning. Anita. Behav.,
32, t257-1259.
Martin, P. & Bateson, P. 1986. Measuring Behaviour.
Cambridge: Cambridge University Press.
Martin, R. D. 1984. Scaling effects and adaptive strategies
in mammalian lactation. Symp. zool. Soc. Lond., 51,
82117.
Melnick, D. J. & Pearl, M. C. 1987. Cercopithecines in
multimale groups: genetic diversity and population
structure. In: Primate Societies (Ed. by B. B. Smuts,
D. L. Cheney, R. M. Seyfarth, R. W. Wrangham &
T. T. Struhsaker), pp. 121-134. Chicago: The University
of Chicago Press.
Mori, A. 1979. Analysis of population changes by
measurements of body weight in the Koshima troop of
Japanese monkeys. Primates, 20, 371-397.
Nash, L. T. 1978. The development of the mother-infant
relationship in wild baboons (Papio anubis). Anim.
Behav., 26, 746-759.
Nicolson, N. A. 1982. Weaning and the development of
independence in olive baboons. Ph.D. thesis, Harvard
University.
Nicolson, N. A. 1987. Infants, mothers, and other females.
In: Primate Societies (Ed. by B. B. Smuts, D. L. Cheney,
R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker),
pp. 330 342. Chicago: The University of Chicago Press.
Oftedal, O. T. 1984. Milk composition, milk yield and
energy output at peak lactation: a comparative review.
Symp. zool. Soc. Lond., 51, 33-85.
Parker, G. A. & MacNair, M. R. 1978. Models of parenW
offspring conflict: I. Monogamy. Anita. Behav., 26,
97-110.
Parker, G. A. & MacNair, M, R. 1979. Models of
parent-offspring conflict. IV. Suppression: evolution-
ary retaliation by the perent. Anita. Behav., 27,
121~1235.
Prentice, A. M. & Whitehead, R. G. 1987. The energetics
of human reproduction. Syrup. zool. Soc. Lond., 57,
275-304.
Silk, J. B. 1988. Maternal investment in captive bonnet
macaques (Macaca radiata). Am. Nat., 132, 1-19.
Silk, J. B., Samuels, A. & Rodman, P. S. 1981. The
influence of kinship, rank and sex on affiliation and
aggression between adult female and immature bonnet
macaques ( Macaca radiata). Behaviour, 78, 111-137.
Simpson, M. J. A. & Simpson, A. E. 1986. The emergence
and maintenance of interdyad differences in the
mother-infant relationships of rhesus macaques: a
correlational study. Int. J. Primatol., 7, 377-397.
Simpson, M. J. A., Simpson, A. E., Hooley, J. & Zunz,
M. 1981. Infant-related influences on birth intervals in
rhesus monkeys. Nature, Lond., 290, 49-51.
Simpson, M. J. A., Simpson, A. E. & Howe, S. 1986.
Changes in the rhesus mother-infant relationship
through the first four months of life. Anim. Behav., 34,
1528-1539.
Spencer-Booth, Y. 1969. The behaviour of twin rhesus
monkeys and comparisons with the behaviour of single
infants. Primates, 9, 75-84.
Stamps, J. A., Clark, A., Kus, B. & Arrowood, P. 1985.
Paren~offspring conflict in budgerigars. Behaviour, 94,
140.
Stamps, J. A., Metcalf, R. A. & Krishnan, V. V. 1978. A
genetic analysis of parent-offspring conflict. Behav.
Ecol. Sociobiol., 3, 369-392.
 Gomendio: Parent~offspring conflict in macaques
Stewart, K. 1988. Suckling and lactational anoestrus in
. wild gorillas. J. Reprod. Fert., 83, 627-634.
Trillmich, F. 1990. The behavioral ecology of maternal
effort in fur seals and sea lions. Behaviour, 114, 3 20.
Trivets, R. L. 1972. Parental investment and sexual selec-
tion. In: Sexual Selection and the Descent of Man (Ed.
by B. Campbell), pp. 136-179. Chicago: Aldine.
Trivers, R. L. 1974. Parent-offspring conflict. Am. Zool.,
14, 249-264.
Trivets, R. L. 1985. Social Evolution. Menlo Park,
California: The Benjamin/Cummins Publishing
Company.
Vandenbergh, J. G. & Vessey, S. H. 1968. Seasonal breed-
ing of free-ranging rhesus monkeys and related ecologi-
cal factors. J. Reprod. Fert., 15, 71-79.
1005
van Wagenen, G. 1972. Vital statistics from a breeding
colony: reproductive and pregnancy outcome in
Macaca mulatta. J. Med. Primatol., 1, 3 28.
Walker, M. L., Gordon, T. P. & Wilson, M. E. 1983.
Menstrual cycle characteristics of seasonally breeding
rhesus monkeys. Biol. Reprod., 29, 841-848.
Wilson, M. E , Walker, M. L., Pope, N. S. & Gordon,
T. P. 1988. Prolonged lactational infertility in
adolescent rhesus monkeys. Biol. Reprod., 38,
163 174.
Worlein, J. M., Eaton, G. G., Johnson, D. F. & Glick,
B. B. 1988. Mating season effects on mother-infant
conflict in Japanese macaques, Macacafuscata. Anita.
Behav., 36, 1472-1481.